Baculovirus VP80 protein and the F-actin cytoskeleton interact and connect the viral replication factory with the nuclear periphery

Journal of Virology

Volumn 85, Issue 11, 2011, Pages 5350-5362

  Marek, Martin ^a,b,c   Merten, Otto Wilhelm ^b   Galibert, Lionel ^b   Vlak, Just M ^a   van Oers, Monique M ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b GÉNÉTHON   (France)

^c INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; F ACTIN; PARAMYOSIN; PROTEIN VP80; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; BACULOVIRUS; CELL MEMBRANE; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSKELETON; IMMUNOPRECIPITATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; VIRUS NUCLEOCAPSID; VIRUS REPLICATION;

ACTINS; ANIMALS; ARTIFICIAL GENE FUSION; CAPSID PROTEINS; CELL LINE; CELL NUCLEUS; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HOST-PATHOGEN INTERACTIONS; IMMUNOPRECIPITATION; LEPIDOPTERA; NUCLEOPOLYHEDROVIRUS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; STAINING AND LABELING;

AUTOGRAPHA CALIFORNICA; AUTOGRAPHA CALIFORNICA NUCLEOPOLYHEDROVIRUS; INVERTEBRATA; NUCLEOPOLYHEDROVIRUS;

EID: 79956115024     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00035-11     Document Type: Article

References (63)

1. Abramoff, M. D., P. J. Magelhaes, and S. J. Ram. 2004. Image processing with ImageJ. Biophotonics Int. 11:36-42.
2. Altschul, S., et al. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
3. Appel, R. D., A. Bairoch, and D. F. Hochstrasser. 1994. A new generation of information retrieval tools for biologists: the example of the ExPASy WWW server. Trends Biochem. Sci. 19:258.
4. Ayres, M. D., S. C. Howard, J. Kuzio, M. Lopez-Ferber, and R. D. Possee. 1994. The complete DNA sequence of Autographa californica nuclear polyhedrosis virus. Virology 202:586-605.
5. Bolte, S., and F. P. Cordelires. 2006. A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 224:213-232.
6. Braunagel, S. C., W. K. Russell, G. Rosas-Acosta, D. H. Russell, and M. D. Summers. 2003. Determination of the protein composition of the occlusionderived virus of Autographa californica nucleopolyhedrovirus. Proc. Natl. Acad. Sci. U. S. A. 100:9797-9802.
7. Braunagel, S. C., and M. D. Summers. 1994. Autographa californica nuclear polyhedrosis virus, PDV, and ECV viral envelopes and nucleocapsids: structural proteins, antigens, lipid and fatty acid profiles. Virology 202:315-328.
8. Carstens, E. B. 2009. AcMNPV as a model for baculovirus DNA replication. Virol. Sin. 24:243-267.
9. Charlton, C. A., and L. E. Volkman. 1993. Penetration of Autographa californica nuclear polyhedrosis virus nucleocapsids into IPLB Sf21 cells induces actin cable formation. Virology 197:245-254.
10. Charlton, C. A., and L. E. Volkman. 1991. Sequential rearrangement and nuclear polymerization of actin in baculovirus-infected Spodoptera frugiperda cells. J. Virol. 65:1219-1227.
11. Cisterna, B., D. Necchi, E. Prosperi, and M. Biggiogera. 2006. Small ribosomal subunits associate with nuclear myosin and actin in transit to the nuclear pores. FASEB J. 20:1901-1903.
12. Cohen, D. P. A., M. Marek, B. G. Davies, J. M. Vlak, and M. M. van Oers. 2009. Encyclopedia of Autographa californica nucleopolyhedrovirus genes. Virol. Sin. 24:359-414.
13. de Castro, E., et al. 2006. ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Res. 34:W362-W365.
14. Dong, S., et al. 2010. Autographa californica multicapsid nucleopolyhedrovirus efficiently infects Sf9 cells and transduces mammalian cells via direct fusion with the plasma membrane at low pH. J. Virol. 84:5351-5359.
15. Duan, J., et al. 2010. SilkDB v2.0: a platform for silkworm (Bombyx mori) genome biology. Nucleic Acids Res. 38:D453-D456.
16. Edgar, R. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
17. Epstein, H. F., B. J. Aronow, and H. E. Harris. 1976. Myosin-paramyosin cofilaments: enzymatic interactions with F-actin. Proc. Natl. Acad. Sci. U. S. A. 73:3015-3019.
18. Fang, M., Y. Nie, and D. A. Theilmann. 2009. AcMNPV EXON0 (AC141) which is required for the efficient egress of budded virus nucleocapsids interacts with β-tubulin. Virology 385:496-504.
19. Feierbach, B., S. Piccinotti, M. Bisher, W. Denk, and L. W. Enquist. 2006. Alpha-herpesvirus infection induces the formation of nuclear actin filaments. PLoS Pathog. 2:0763-0776.
20. Finn, R. D., et al. 2008. The Pfam protein families database. Nucleic Acids Res. 36:D281-D288.
21. Fraser, M. J. 1986. Ultrastructural observations of virion maturation in Autographa californica nuclear polyhedrosis virus infected Spodoptera frugiperda cell cultures. J. Ultrastruct. Mol. Struct. Res. 95:189-195.
22. Goley, E. D., et al. 2006. Dynamic nuclear actin assembly by Arp2/3 complex and a baculovirus WASP-like protein. Science 314:464-467.
23. Hooper, S. L., K. H. Hobbs, and J. B. Thuma. 2008. Invertebrate muscles: thin and thick filament structure; molecular basis of contraction and its regulation, catch and asynchronous muscle. Prog. Neurobiol. 86:72-127.
24. Jen, D., et al. 2004. ImageSurfer: a tool for visualizing correlations between two volume scalar fields. In Proceedings of the Conference on Visualization (2004). http://wwwx.cs.unc.edu/~taylorr/Comp715/papers/imagesurfer.pdf.
25. Ke, J., J. Wang, R. Deng, Z. Wang. 2008. Autographa californica multiple nucleopolyhedrovirus ac66 is required for the efficient egress of nucleocapsids from the nucleus, general synthesis of preoccluded virions and occlusion body formation. Virology 374:421-431.
26. Kool, M., C. H. Ahrens, J. M. Vlak, and G. F. Rohrmann. 1995. Replication of baculovirus DNA. J. Gen. Virol. 76:2103-2118.
27. Lanier, L. M., and L. E. Volkman. 1998. Actin binding and nucleation by Autographa californica M nucleopolyhedrovirus. Virology 243:167-177.
28. Lehmann, M. J., N. M. Sherer, C. B. Marks, M. Pypaert, and W. Mothes. 2005. Actin- and myosin-driven movement of viruses along filopodia precedes their entry into cells. J. Cell Biol. 170:317-325.
29. Letunic, I., et al. 2006. SMART 5: domains in the context of genomes and networks. Nucleic Acids Res. 34:D257-D260.
30. Letunic, I., T. Doerks, and P. Bork. 2009. SMART 6: recent updates and new developments. Nucleic Acids Res. 37:D229-D232.
31. Li, K., et al. 2010. The putative pocket protein binding site of Autographa californica nucleopolyhedrovirus BV/ODV-C42 is required for virus-induced nuclear actin polymerization. J. Virol. 84:7857-7868.
32. Li, Q., and S. K. Sarna. 2009. Nuclear myosin II regulates the assembly of preinitiation complex for ICAM-1 gene transcription. Gastroenterology 137: 1051-1060.
33. Li, X., A. Pang, H. A. M. Lauzon, S. S. Sohi, and B. M. Arif. 1997. The gene encoding the capsid protein P82 of the Choristoneura fumiferana multicapsid nucleopolyhedrovirus: sequencing, transcription and characterization by immunoblot analysis. J. Gen. Virol. 78:2665-2673.
34. Long, G., X. Pan, R. Kormelink, and J. M. Vlak. 2006. Functional entry of baculovirus into insect and mammalian cells is dependent on clathrin-mediated endocytosis. J. Virol. 80:8830-8833.
35. Lu, A., and E. B. Carstens. 1992. Nucleotide sequence and transcriptional analysis of the p80 gene of Autographa californica nuclear polyhedrosis virus: a homologue of the Orgyia pseudotsugata nuclear polyhedrosis virus capsidassociated gene. Virology 190:201-209.
36. Lu, A., and L. Miller. 1995. The roles of eighteen baculovirus late expression factor genes in transcription and DNA replication. J. Virol. 69:975-982.
37. Marchler-Bauer, A., et al. 2005. CDD: a conserved domain database for protein classification. Nucleic Acids Res. 33:D192-D196.
38. Marchler-Bauer, A., et al. 2003. CDD: a curated Entrez database of conserved domain alignments. Nucleic Acids Res. 31:383-387.
39. Marek, M., M. M. van Oers, F. F. Deveraj, J. M. Vlak, and O.-W. Merten. 2011. Engineering of baculovirus vectors for the manufacture of virion-free biopharmaceuticals. Biotechnol. Bioeng. 108:1056-1067.
40. Muller, R., M. N. Pearson, R. L. Q. Russell, and G. F. Rohrmann. 1990. A capsid-associated protein of the multicapsid nuclear polyhedrosis virus of Orgyia pseudotsugata: genetic location, sequence, transcriptional mapping, and immunocytochemical characterization. Virology 176:133-144.
41. Ohkawa, T., and L. E. Volkman. 1999. Nuclear F-actin is required for AcMNPV nucleocapsid morphogenesis. Virology 264:1-4.
42. Ohkawa, T., L. E. Volkman, and M. D. Welch. 2010. Actin-based motility drives baculovirus transit to the nucleus and cell surface. J. Cell Biol. 190: 187-195.
43. Pagni, M., et al. 2004. MyHits: a new interactive resource for protein annotation and domain identification. Nucleic Acids Res. 32:W332-W335.
44. Pagni, M., et al. 2007. MyHits: improvements to an interactive resource for analyzing protein sequences. Nucleic Acids Res. 35:W433-W437.
45. Passarelli, A. L., and L. A. Guarino. 2007. Baculovirus late and very late gene regulation. Curr. Drug Targets 8:1103-1115.
46. Peng, K., et al. 2009. Identification of protein-protein interactions of the occlusion-derived virus-associated proteins of Helicoverpa armigera nucleopolyhedrovirus. J. Gen. Virol. 91:659-670.
47. Pettersen, E. F., et al. 2004. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25:1605-1612.
48. Roberts, K. L., and J. D. Baines. 2010. Myosin Va enhances secretion of herpes simplex virus 1 virions and cell surface expression of viral glycoproteins. J. Virol. 84:9889-9896.
49. Schultz, J., F. Milpetz, P. Bork, and C. P. Ponting. 1998. SMART, a simple modular architecture research tool: identification of signaling domains. Proc. Natl. Acad. Sci. U. S. A. 95:5857-5864.
50. Slack, J., and B. M. Arif. 2007. The baculoviruses occlusion-derived virus: virion structure and function. Adv. Virus Res. 69:99-165.
51. Summers, M. D., and L. E. Volkman. 1976. Comparison of biophysical and morphological properties of occluded and extracellular nonoccluded baculovirus from in vivo and in vitro host systems. J. Virol. 17:962-972.
52. Tang, X.-D., et al. 2008. Characterization of a Bombyx mori nucleopolyhedrovirus with Bmvp80 disruption. Virus Res. 138:81-88.
53. Vanarsdall, A. L., K. Okano, and G. F. Rohrmann. 2006. Characterization of the role of very late expression factor 1 in baculovirus capsid structure and DNA processing. J. Virol. 80:1724-1733.
54. Vialard, J. E., and C. D. Richardson. 1993. The 1,629-nucleotide open reading frame located downstream of the Autographa californica nuclear polyhedrosis virus polyhedrin gene encodes a nucleocapsid-associated phosphoprotein. J. Virol. 67:5859-5866.
55. Volkman, L. E. 1988. Autographa californica MNPV nucleocapsid assembly: inhibition by cytochalasin D. Virology 163:547-553.
56. Volkman, L. E. 2007. Baculovirus infectivity and the actin cytoskeleton. Curr. Drug Targets 8:1075-1083.
57. Wang, M., et al. 2010. Partial functional rescue of Helicoverpa armigera single nucleocapsid nucleopolyhedrovirus infectivity by replacement of F protein with GP64 from Autographa californica multicapsid nucleopolyhedrovirus. J. Virol. 84:11505-11514.
58. Wang, R., et al. 2010. Proteomics of the Autographa californica nucleopolyhedrovirus budded virions. J. Virol. 84:7233-7242.
59. Waterhouse, A. M., J. B. Procter, D. M. A. Martin, M. Clamp, and G. J. Barton. 2009. Jalview version 2. A multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189-1191.
60. Wu, W., et al. 2008. Autographa californica multiple nucleopolyhedrovirus 38K is a novel nucleocapsid protein that interacts with VP1054, VP39, VP80, and itself. J. Virol. 82:12356-122354.
61. Xu, F., J. M. Vlak, A. P. M. Eker, and M. M. van Oers. 2010. DNA photolyases of Chrysodeixis chalcites nucleopolyhedrovirus target to the nucleus and interact with chromosomes and mitotic spindle structures. J. Gen. Virol. 91:907-914.
62. Xu, X., et al. 2011. VP15R from infectious spleen and kidney necrosis virus is a non-muscle myosin-II-binding protein. Arch. Virol. 156:53-61.
63. Ye, J., J. Zhao, U. Hoffmann-Rohrer, and I. Grummt. 2008. Nuclear myosin I acts in concert with polymeric actin to drive RNA polymerase I transcription. Genes Dev. 22:322-330.